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Journal of Human Kinetics volume 43/2014, 97-104 DOI: 10.2478/hukin-2014-0094 97
Physical Activity, Sport & Health
1 - Integrated Colleges of Northern Minas Gerais – Funorte, Brazil. 2 - University of Tras-os-Montes and Alto Douro, Vila Real, Portugal. 3 - University President Antônio Carlos - UNIPAC, Uberlândia, MG, Brazil. 4 - Fire Department of the State of Minas Gerais, 5th Battalion Fire Department, Uberlândia, MG, Brazil. 5 - University Center Triangle - UNITRI, Uberlândia, MG, Brazil.
.
Authors submitted their contribution to the article to the editorial board.
Accepted for printing in the Journal of Human Kinetics vol. 43/2014 on November 2014.
Nutritional Status Associated with Metabolic Syndrome
in Middle-School Children
in the City of Montes Claros - MG, Brazil
by
Igor Raineh Durães Cruz1,2, Daniella Mota Mourão1,2, Daniel Antunes Freitas1,
Andrey George Silva Souza1,2, Alessandra Ribeiro Pereira1,2, Felipe José Aidar2,3,4,5,
André Luiz Gomes Carneiro2,3
The aim of this study was to investigate the association between nutritional status and prevalence of metabolic
syndrome (MS) in middle-school students in the city of Montes Claros - MG. The sample consisted of 382 students,
aged 10-16 years. Nutritional status was evaluated using the Body Mass Index (BMI). Metabolic syndrome (MS) was
defined as the presence of two or more criteria in accordance with definition of the International Diabetes Federation.
The overall prevalence of MS was 7.9%. 9.7% of students with MS were overweight and 72.4% were obese. Therefore,
it can be inferred that carrying excess weight considerably increases the chances for a child to develop MS, and
concomitantly increases the child’s risk for developing cardiovascular disease.
Key words: dyslipidemia, metabolic syndrome, children, cross-sectional study, youth.
Introduction Metabolic syndrome (MS) is defined by
the presence of risk factors such as high blood
pressure, abdominal obesity,
hypertriglyceridemia, low concentration of high
density lipoprotein (HDL-c) and hyperglycemia
(Eckel et al., 2005; Oda, 2012; Chiu et al., 2012).
Prevalence of MS has increased among children,
adolescents and adults, and is closely related to
the presence of excess weight or obesity (Cruz
and Goran, 2004; Zimmet et al., 2007).
No consensus has been reached in the
literature regarding the diagnosis of MS in
pediatric populations because blood pressure
(BP), lipid profile and anthropometric values vary
with age and maturity, requiring different cutoff
points to account for variations in age, sex and
other criteria (Damiani et al., 2011). However, the
International Diabetes Federation (IDF) has
established criteria for identifying SM in children
and teenagers, dividing them into three groups: 6
to < 10 years old, 10 to 16 years old and > 16 years
old (Zimmet et al., 2007; Damiani et al., 2011). In
accordance with the criteria of the IDF, MS is a
combination of abdominal obesity and one or
more other risk factors (Zimmet et al., 2007).
Studies using the cutoff points established
by the IDF indicate the presence of MS in 16.3% of
children living in Malaysia (Zimmet et al., 2007),
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4.6% of adolescents in Vietnam (Nguyen et al.,
2011), 33% in Turkey (Sagun et al., 2011), and
39.7% of a municipal population in Brazil (Costa
et al., 2012).
Investigations of various methodologies
concur that MS is associated with cardiovascular
diseases (CVD) regardless of age, and that excess
weight or obesity is the most prevalent risk factor
(Cobayashi et al., 2010; Armas et al., 2012). Thus,
as the incidence of childhood obesity is rising, the
prevalence of MS in this population is also
increasing (Pacífico et al., 2011) and needs to be
futher investigated in the Brazilian pediatric
population (Silva et al., 2012; Stabelini et al., 2012).
The aim of this study was to investigate
the association between nutritional status and
prevalence of metabolic syndrome in middle-
school children in the city of Montes Claros, MG,
Brazil.
Material and Methods
The sample was determined in two stages:
1) stratification of elementary school students (n =
53.032) and middle school students (n = 15.505),
and 2) clustering of schools according to the four
regions of the city: north (n = 10), south (n = 17),
east (n = 15), west (n = 13), totaling 55 schools.
Four schools (one from each region) were
randomly drawn in order to minimize the
logistical difficulties of displacement while
acquiring a sufficient number of students to
constitute the sample. At each of these randomly
selected schools, all students between the ages of
10 and 16 years old who participated in physical
education classes were invited to take part in the
study. The calculation of the final sample was
established with a margin of error of three
percentage points and a confidence level of 95%, a
design effect of 1.5 plus 10% for possible losses
and / or refusals. Thus, 421 children were selected
using the formula: n = (ZZ).p.q.N/e.e.(N-1)+
p.q.Z.Z, where Z = confidence interval, P =
probability of being rejected 50%, q = probability
of being chosen, 50% N= population and e =
percentage of error ≤ 0.05 (Almeida and Freire,
2003; Cruz et al., 2014).
Of the 421 students initially selected, 15
students (12 boys and 3 girls) did not obtain the
signature of a parent or guardian on the consent
form; 4 children (3 boys and 1 girl) did not
properly complete the questionnaire; 12 students
(3 boys and 9 girls) did not complete the physical
examination; and 8 male students were randomly
excluded, reaching the final sample of 382
students distributed in the following regions:
north (n = 62), south (n = 111), east (n = 105) and
west (n = 104).
Informed consent to participate in the
study was signed by a parent or guardian of every
student included in the results of the study. The
study was approved by the Institutional Review
Board of the State University of Montes Claros
(process no. 152.330/12). Participants were duly
informed about the study and signed informed
consent forms in accordance with Resolution
196/1996 of the Brazilian National Health Council,
and in accordance with the ethical principles
contained in the Declaration of Helsinki (1964,
revised in 1975, 1983, 1989, 1996 and 2000).
Instruments
Socioeconomic status (CSE) of
participants in the sample was attained by means
of a structured questionnaire which took into
account the educational background of parents,
skin color of the children and family income.
Based on this information, participants were
classified into eight groups (A1, A2, B1, B2, C1, C2,
D, E) and these eight groups were assigned to one
of two categories of economic status: high
economic status (A1, A2, B1) or low socioeconomic
status (B2, C1, C2, D and E) (Fernandes et al., 2008).
Variables of nutritional status and metabolic
syndrome
Anthropometry: Body mass (BM) and
height (H) were measured on a medical platform
scale (Filizola, Brazil) with a weight capacity of
150 kg with precision to 100 g and a height
capacity of 2 m with precision to 0.1 cm. The
subject stood with his or her arms along the body
and with his or her head positioned in the
Frankfurt plane. Nutritional status was defined by
the Body Mass Index (BMI) and classified as
normal weight, overweight or obesity (Cole et al.,
2000). Abdominal circumference (AC) was
measured using a flexible metal anthropometric
tape (Sanny SN 40-10, Brazil). The measurements
were performed upon exhalation with the values
on the measurement tape facing the evaluator and
were determined in the horizontal plane. Males
were evaluated at the plane just below the last rib
and females evaluated at the level of the navel
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(Lohman et al., 1998).
Blood pressure (SBP / DBP) - was measured using a
sphygmomanometer (BD, Brazil) and a Rappaport
stethoscope (Premium, Brazil) that was previously
tested and calibrated. The evaluation took place
with the individual in a sitting position after 10
min of rest. The right arm supported at the heart
level was used for the analysis. The first Korotkoff
sound was considered for systolic blood pressure
reading and the last for diastolic blood pressure.
A five minute rest interval was given between the
first and subsequent measurement. The average of
the two measurements was calculated to
minimize measurement biases (BGH, 2010).
Blood samples - blood samples for the biochemical
tests were collected at Santa Clara Laboratory
(Montes Claros, MG, Brazil) through
venipuncture with disposable needles and
syringes, with participants fasting for 12 hours.
Approximately 10 ml of blood was collected in a
test tube without anticoagulants. The test tubes
were labeled with identification tags and stored in
two coolers (®Termolar, Brazil) with a capacity of
200 tubes each. The tubes were placed in a
centrifuge at 3500 rpm for 10 min and stored in a
refrigerator at -20 ° C for later analysis. The
concentrations of triglycerides (TG), high density
cholesterol (HDL-C) and glucose (GLU) were
determined by a calorimetric oxidase enzyme
analyzer provided by Liquiform Diagnostic Kits ®
(Labtest, Brazil).
The International Diabetes Federation (IDF)
created age appropriate definitions and
approaches to the treatment of SM for children
and teenagers, dividing them into groups: 6 to <
10 years, 10 to 16 years and > 16 years. The IDF
recommends that the diagnosis of MS should not
be given to children under the age of 10,
recommending that the child should be counseled
about the need for weight loss and a change of
lifestyle. However, at 10 years or older, the
diagnosis should be given and should be based on
the presence of abdominal obesity and the
presence of two or more of the following
syndromes: TG> 150 mg / dL, HDL <40 mg / dL,
Glu> 100 mg / dL, SBP ≥ 130 and DBP ≥ 85 mmHg
20. For adolescents above the age of 16, the adult
criteria are used (Damiani et al., 2011).
Procedures
The subjects were evaluated by two
physical education teachers with a minimum
experience of 30 ratings. The Pearson values for
intra-rater and inter-rater reliability were 0.975
and 0.967, respectively. Data collection occurred
in four stages. In the first stage, the researcher
presented the objectives of the project to the
directors of the randomly selected schools. The
school directors subsequently informed the
physical education teachers about the study
procedures. Individual participants were
randomly drawn from the population of students
who fulfilled the criteria for inclusion in the
sample. In the second stage, the researcher
presented the randomly selected students with
the informed consent form to be completed by a
parent or guardian and returned the next day. In
the third stage, questionnaires were applied and
anthropometric measurements were completed.
In the fourth stage, the students came to the
laboratory for blood sampling after fasting for 12
hours. The time between each step was a
minimum interval of 24 hours.
Statistics
The Statistical Package for Social Sciences
(SPSS 20.0 for Windows ®) was used to analyze
the data. Descriptive statistics were done through
measures of central tendency mean ± standard
deviation (M ± SD). We applied the chi-square test
in order to associate prevalence of MS with
nutritional status. The magnitude was calculated
from the odds ratio (OR) with confidence
intervals of 95% (95% CI).
Results
Table 1 shows the description of the
sample, categorized by nutritional status.
33.3% of male participants and 66.7% of
female participants were found to be overweight
and 34.5% of male participants and 65.5% of
female participants were found to be obese.
Students under the age of 13 were most affected
by being overweight or obese. BM was greater
among obese children. There were more
overweight and obese children in the elementary
school than in the middle school. Low income
status was associated with children being
overweight or obese.
Table 2 describes the criteria for diagnosis
of MS, categorized by nutritional status.
The results show that being overweight
corresponded with abnormal (greater than
recommended) waist circumference (WC) in
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100 Nutritional status associated with metabolic syndrome in middle-school children
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12.5% of participants and other abnormal values,
increasing the chances of diagnosis of MS, since
the IDF uses the criterion of change in waist
circumference combined with two criteria.
Table 1
Description of the sample categorized by nutritional status. VARIABLES Nutricional Status Total
Normal weight Overweight Obese
Gender
Male 117 (41,6%) 24 (33,3%) 10 (34,5%) 151 (39,5%)
Female 164 (58,4%) 48 (66,7%) 19 (65,5%) 231 (60,5%)
Age
<13 121 (43,1%) 36 (50%) 16 (55,2%) 173 (45,3%)
≥13 160 (56,9%) 36 (50%) 13 (44,8%) 209 (54,7%)
Weight (kg) 44,44 ± 9,63 59,45 ± 10,83 72,79 ± 13,64 49,42 ± 13,51
Height (m) 1,55 ± 0,1 1,57 ± 0,09 1,54 ± 0,93 1,55 ± 0,1
Education
1 st grade/ Elementary school 234 (83,3%) 67 (93,1%) 26 (89,7%) 327 (85,6%)
2 nd grade/High school 47 (16,7%) 5 (6,9%) 3 (10,3%) 55 (14,4%)
Race
Non-white 233 (82,9%) 60 (83,3%) 26 (89,7%) 319 (83,5%)
White 48 (17,1%) 12 (16,7%) 3 (10,3%) 63 (16,5%)
Socio-economic status
HSS 27 (9,6%) 8 (11,1%) 2 (6,9%) 37 (9,7%)
LSS 254 (90,4%) 64 (88,9%) 27 (93,1%) 345 (90,3%)
HSS: High Socioeconomic Status; LSS: Low Socioeconomic Status.
Table 2
Description of MS criteria met according to nutritional status. Variables Nutritional Status
p Normal Overweight Obesity OR CI (95%)
WC (cm)
Normal 281 (100%) 63 (87,5%) 9 (31%)
Abnormal -- 9 (12,5%) 20 (69%) 15,55 (5,43-44,51) 0,000*
SBP (mmHg)
Normal 281 (100%) 72 (100%) 27 (93,1%)
Abnormal -- -- 2 (6,9%) 3,66 (2,65-5,05) 0,024*
DBP (mmHg)
Normal 281 (100%) 72 (100%) 28 (96,6%)
Abnormal -- -- 1 (3,4%) 3,57 (2,6-4,89) 0,113
TG (mg/dL)
Normal 279 (99,3%) 70 (97,2%) 24 (82,8%)
Abnormal 2 (0,7%) 2 (2,8%) 5 (17,2%) 7,29 (1,32-40,07) 0,01*
HDL-c (mg/dL)
Normal 240 (85,4%) 56 (77,8%) 19 (65,5%)
Abnormal 41 (14,6%) 16 (22,2%) 10 (34,5%) 1,84 (0,71-4,74) 0,202
GLU (mg/dL)
Normal 278 (98,9%) 72 (100%) 27 (93,1%)
Abnormal 3 (1,1%) -- 2 (6,9%) 3,66 (2,65-5,058) 0,024*
OR: odds ratio, CI: confidence interval. p: statistical significance from the chi-square test.
CA: waist circumference, SBP: systolic blood pressure, DBP: diastolic blood pressure,
TG: triglycerides, HDL-C: High Density Cholesterol, GLU: glucose.
*p<0,05
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Table 3
Description of prevalence (%) of MS with 95% confidence, according to nutritional status. Variables Nutritional Status
p Normal Overweight Obesity OR CI (95%)
Metabolic
Syndrome
Absent 279 (99,3%) 65 (90,3%) 8 (27,6%)
Present 2 (0,7%) 7 (9,7%) 21 (72,4%) 24,37 (7,89-75,25) 0,000*
OR: odds ratio, CI: confidence interval. p: statistical significance from the chi-square test.
*p<0,05
Students with obesity had a greater
tendency towards abnormal values for the WC
(OR = 15.55, CI: 5.43 to 44.51, p = 0.001), SBP (OR =
3.66, CI: 2, 65 to 5.05, p = 0.024), TG (OR = 7.29, CI:
1.32 to 40.07, p = 0.01) and GLU (OR = 3.66, CI:
2.65 -5.058, p = 0.024). The differences in risk
factors between obese and normal weight children
were significant, revealing a strong association
between obesity and metabolic syndrome.
Table 3 describes prevalence of MS and its
association with the nutritional status of
schoolchildren in the city of Montes Claros.
The overall prevalence of MS was 7.9% in
the sample of school children. However, only
0.7% of normal weight children and 9.7% of
overweight children had MS, while 72.4% of obese
children fulfilled the criteria for diagnosis of MS.
This significant association (p = 0.001)
demonstrates that the obese children were 24.37
times more likely to meet the criteria for diagnosis
of MS (CI: 7.89 to 75.25).
Discussion
The aim of this study was to investigate
the association between nutritional status and
prevalence of metabolic syndrome (MS) in
middle-school children. The data from this study
showed higher prevalence of excess weight or
obesity among female students, indicating that
girls are more likely to develop MS than boys.
This corresponds to a similar study of 5913
participants in the United States in which females
had a higher frequency of being overweight or
obese when compared to males (Maty et al., 2008).
The relative values of height and weight
are considered in the calculation of the BMI. In
this way, a more comprehensive view considers
that both height and age need to be considered
when evaluating whether a child is overweight or
obese. When a child is heavy for their height and
age, slow and steady weight loss are
recommended to reduce the BMI and minimize
cardiovascular risk (Terres et al., 2006; Kassi et al.,
2011).
In several studies it has been noted that
education reduces or eliminates certain risk
factors. For example, one study showed a
significant negative association between lower
levels of education and excess weight or obesity.
This study relates that when parents have only
five to eight years of schooling, the risk of their
children being overweight or obese is 2.53 (CI:
1.32 to 4.85) times higher than amongst children
whose parents have at least a high school
education (Terres et al., 2006). Another study
found that children tended to lose excess weight
during high school when they were exposed to
nutritional knowledge and tools to control weight
(Barrington et al., 2010).
The present study found that non-white
and low income children had higher incidences of
being overweight or obese. Since non-white status
is associated with lower incomes in Brazil, the
similarity in these associations are related (Ribeiro
et al., 2009). Similarly, a longitudinal study
conducted with 29,146 Americans between 2 to 17
years showed more excess weight among black
and Hispanic when compared with white
children. The association between racial identity
and nutritional status is considered to be a by-
product of unequal educational and vocational
opportunities and cultural differences (Freedman
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et al., 2006). Numerous studies have associated
lower socioeconomic status with obesity,
hypertension and dyslipidemia (Kassi et al., 2011;
Ribeiro et al., 2009).
Similar studies support a relationship
between increased (abnormal) waist
circumference (WC) and prevalence of children
being overweight (12.5%) or obese (69%) and
demonstrate that a high level of abdominal fat in
childhood is related to insulin resistance,
dyslipidemia and hypertension (Johnson et al.,
2010). A recent study conducted in 991 schools in
Paraná, Brazil showed that female students had a
tendency toward abnormally high values for
waist circumference and that this was related to
the intake of excess sugar, limited physical
inactivity, unhealthy family life styles and low
socioeconomic status (Moraes et al., 2013).
BMI and WC are widely used as
predictors of nutritional status, but the IDF also
uses blood pressure as an essential criterion for
diagnosis of MS (Reaven, 2006). Individuals with
high BMI tend to have 3.6 and 2.7 times the risk of
change in SBP and DBP, respectively (Ribeiro et
al., 2006). Studies have demonstrated that
elevated BP in childhood and adolescence is
associated with anthropometric changes and a
higher incidence of MS in adulthood (Ribeiro et
al., 2006).
High concentrations of triglycerides
present a picture of hypertriglyceridemia, which
contributes to decreases in HDL-C and the
production of LDL cholesterol particles. These
changes result in an atherogenic lipoprotein
profile congruent with an increased risk of
cardiovascular disease (Moraes and Falcão, 2013;
Reaven, 2006; Benmohammed et al., 2011). A case-
control study of adolescents living in Malaysia
indicated that being overweight or obese affects
the odds of having high triglycerides by 12% and
similarly resulted in a 2.5 times greater chance of
developing MS (Costa et al., 2012).
Hyperglycemia was detected in 6.9% of
children with obesity. It is possible that this
relatively low prevalence could be inaccurate as
the study did not investigate the use of
hypeglycemic or diabetic medications among
children in the sample. The IDF emphasizes the
importance of measuring the fasting glucose as it
is a more accurate measure of risk for MS
(Zimmet et al., 2007). Another study suggests that
hyperglycemia may not be concurrent with MS as
it may occur later, when the function of the
pancreas is challenged because of ongoing efforts
to keep normal glucose levels through increased
insulin production (Ferrannini and Iozzo, 2006).
While it is not advisable to use glucose levels as a
sole indicator of MS since studies of this
relationship present a wide variety of criteria, the
existent literature uniformly supports the
presence of a positive association between
increased glucose levels and higher prevalence of
being overweight or obese (Moraes and Falcão,
2013; Papoutsakis et al., 2012).
In our study, 0.7% of normal weight, 9.7%
of overweight and 72.4% of obese children met the
criteria for MS, indicating that nutritional status
plays a key role in its incidence. A case-control
study with 402 children living in Malaysia found
prevalence of MS of 16.3% among obese children
and 5.3% among overweight children (Wee et al.,
2011). Similarly, the relationship between MS and
nutritional status was investigated in 693 high
school students, finding prevalence of 4.6% and
11.8% among overweight and obese adolescents
(Cobayashi et al., 2012). Our findings are also in
agreement with the results of a cross-sectional
survey conducted with 133 subjects of an
endocrinology clinic that indicated the influence
of obesity on the occurrence of MS, pointing out
that one in five obese patients met three or more
criteria for diagnosis of MS (Nguyen et al., 2010).
In research conducted with hospitalized children
and adolescents with leukemia in Saudia Arabia,
MS was diagnosed in 7.1% of the total sample
with higher incidences among overweight and
obese subjects (Aldhafiri et al., 2012).
An important limitation of the present
study was that as a cross-sectional study, it was
only capable of describing the current status of
the participating children and adolescents and,
therefore, it was not capable of illuminating the
causes and consequences of the problem
Conclusion
In conclusion, nutritional status tends to
be associated with MS among school children,
with prevalence of 0.7% for normal weight
students, 9.7% for overweight students and 72.4%
for obese students in the study population,
leading to the conclusion that obese participants
were 24.37 times more likely to be diagnosed with
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MS, which implies a much higher degree of risk
for cardiovascular disease.
Practical Applications
This study confirmed an association
between metabolic syndrome (MS) and being
overweight or obese amongst school children in
Montes Claros, Brazil. This indicates a great need
for effective educational programs that promote
an increase in physical activity and education in
good nutrition. MS can be avoided by the
adaption of better physical education programs in
school, afterschool and on the weekends. This
study indicates a need for public policies that
incorporate health education in public
programming and quality public and private
education. A mere 30 minutes of physical activity
three times a week could make a significant
difference in the incidence of overweight and
obese children, and, subsequently, reduce the risk
of developing Metabolic Syndrome and
consequent cardiovascular diseases.
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Corresponding author:
Igor Raineh Durães Cruz
Integrated Colleges of Northern Minas Gerais – Funorte, Brazil - Rua Geovane Soares Cruz 93, Lourdes –
cep: 39401482 – Montes Claros, MG, Brazil.
Phone number: +55 38 91638230; E-mail: [email protected]
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